Riva2018 PDF

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 15

CYBERPSYCHOLOGY, BEHAVIOR, AND SOCIAL NETWORKING

Volume X, Number X, 2018


Mary Ann Liebert, Inc.
DOI: 10.1089/cyber.2017.29099.gri

Neuroscience of Virtual Reality:


From Virtual Exposure to Embodied Medicine

Giuseppe Riva, PhD,1,2 Brenda K. Wiederhold, PhD, MBA, BCB, BCN,3,4 and Fabrizia Mantovani, PhD5

Abstract

Is virtual reality (VR) already a reality in behavioral health? To answer this question, a meta-review was
conducted to assess the meta-analyses and systematic and narrative reviews published in this field in the last
twenty-two months. Twenty-five different articles demonstrated the clinical potential of this technology in both
the diagnosis and the treatment of mental health disorders: VR compares favorably to existing treatments in
anxiety disorders, eating and weight disorders, and pain management, with long-term effects that generalize to
the real world. But why is VR so effective? Here, the following answer is suggested: VR shares with the brain
the same basic mechanism: embodied simulations. According to neuroscience, to regulate and control the body
in the world effectively, the brain creates an embodied simulation of the body in the world used to represent and
predict actions, concepts, and emotions. VR works in a similar way: the VR experience tries to predict the
sensory consequences of an individual’s movements, providing to him/her the same scene he/she will see in the
real world. To achieve this, the VR system, like the brain, maintains a model (simulation) of the body and the
space around it. If the presence in the body is the outcome of different embodied simulations, concepts are
embodied simulations, and VR is an embodied technology, this suggests a new clinical approach discussed in
this article: the possibility of altering the experience of the body and facilitating cognitive modeling/change by
designing targeted virtual environments able to simulate both the external and the internal world/body.

Virtual Reality in Behavioral Health: A Meta-Review contribution in many different areas, from anxiety and eating
disorders to psychosis and addiction.

T his special issue presented and discussed different


virtual reality (VR) applications for behavioral health. But
is VR already a reality in behavioral health? To answer this
The most common use of VR in behavioral health is for
exposure therapy (VR exposure [VRE]). VRE is similar to
classic exposure therapy10,16,26—the patient is exposed to a
question, a meta-review was conducted to assess the meta- graded exposure hierarchy—with the only difference being
analyses and systematic and narrative reviews (see Fig. 1 for that VR is substituted for other exposure techniques (e.g.,
the methodology) published in this field in the last 22 months. in vivo or imaginal exposure). In the treatment of complex
Twenty-five different articles1–25 (see Table 1 for the ar- anxiety disorders, the use of VRE is often combined with
ticles’ list and a summary of their conclusions) demonstrated other techniques such as breathing or relaxation exercises,27
the clinical potential of this technology in both the diagno- attentional and autonomic control training,28 biofeedback,29,30
sis and the treatment of mental health disorders. Nine arti- and/or cognitive restructuring.31
cles1,2,6,9,14,15,19,18,22 reviewed the available literature on the Five articles,5,8,10 including a meta-analysis,11,16 spe-
effectiveness of VR in psychiatric/mental health treatment. cifically explored the use of VRE in the treatment of anx-
All of the articles suggest that VR is suitable for the treat- iety disorders. The available data show that VR is able to
ment of mental health problems and could make an important reduce anxiety symptoms significantly in different anxiety

1
Applied Technology for Neuro-Psychology Lab, IRCCS Istituto Auxologico Italiano, Milan, Italy.
2
Department of Psychology, Università Cattolica del Sacro Cuore, Milan, Italy.
3
Virtual Reality Medical Center, La Jolla, California.
4
Virtual Reality Medical Institute, Brussels, Belgium.
5
Department of Human Sciences for Education, Università degli Studi di Milano-Bicocca, Milan, Italy.
ª Giuseppe Riva et al. 2018; Published by Mary Ann Liebert, Inc. This Open Access article is distributed under the terms of the Creative
Commons License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any
medium, provided the original work is properly cited.

1
2 RIVA ET AL.

Articles identified through database


searching (N = 1,220) Number of duplicates (N = 345)

Articles screened after duplicates Articles not meeting inclusion


removed (N = 875) criteria (N = 848)

Reasons for exclusion: review had


Full-text articles assessed for a limited focus on virtual reality
eligibility (N = 27) (N = 2)

Studies included in qualitative


synthesis (N = 25)

FIG. 1. Meta-review methodology. Using the Google Scholar and Scopus databases, a systematic search was conducted to
identify reviews (both systematic and narrative) and meta-analyses that reported on the effects of virtual reality (VR) in the
assessment and treatment in behavioral health: anxiety disorders, pain management, schizophrenia spectrum disorders,
eating and weight disorders, autism spectrum disorders, personality disorders, and substance use disorders. Guidelines for
conducting a systematic review discussed by Uman162 were followed. The ‘‘free-form’’ question was as follows: ‘‘Do
virtual environments perform equal-to-or-better-than traditional modalities in behavioral health?’’ The outcome of interest
was reviews and meta-analyses answering this question in any area of behavioral health. The following search terms were
used: ((‘‘Virtual Reality’’ AND (‘‘Review’’ OR ‘‘Meta-analysis’’ OR ‘‘metaanalysis’’)) AND (‘‘anxiety’’ OR ‘‘phobia’’ OR
‘‘fear’’ OR ‘‘stress’’ OR ‘‘pain’’ OR ‘‘schizophrenia’’ OR ‘‘psychosis’’ OR ‘‘obesity’’ OR ‘‘eating disorders’’ OR ‘‘bu-
limia’’ OR ‘‘binge eating’’ OR ‘‘anorexia’’, OR ‘‘autism’’ OR ‘‘Asperger’’ OR ‘‘substance’’ OR ‘‘drug’’ OR ‘‘nicotine’’
OR ‘‘cocaine’’ OR ‘‘opioids’’). The search targeted articles published between November 2, 2016, and August 1, 2018.
Inclusion criteria included (a) reviews or meta-analyses, (b) English language journals, and (c) peer-reviewed journals.
Exclusion criteria included (a) articles related to the use of VR in surgery or in physical and cognitive rehabilitation; and (b)
articles lacking basic information about the selection of the discussed articles. The meta-review flow diagram is shown.

disorders: phobias,32 post-traumatic stress disorders,33 panic ‘‘body swapping’’51,52—VR is used to induce the illusory
disorder and agoraphobia,34 social anxiety disorders,35 psy- feeling of ownership of a virtual body with a different shape
chological stress,36 and generalized anxiety disorders.37 and/or size. Even if the number of available controlled stud-
The clinical outcome is generally superior to waitlist con- ies is less than for anxiety disorders, the field has rapidly
trol conditions and comparable to in vivo exposure-based evolved.17 Specifically, four different randomized controlled
interventions. trials—one with eating disorders,53 one with morbid obesity,54
A second group of five articles3,12,13,17,23 evaluated the one with binge-eating,55 and one with binge-eating and
efficacy of VR in the treatment of eating and weight disor- bulimia56—have shown after 6-month and 12-month follow-
ders. In this field, VR is used in two different ways.38 First, ups that VR had a higher efficacy than the gold standard in the
VR cue exposure to critical stimuli (e.g., food or human field, that is, cognitive–behavioral therapy.
bodies) allows both a reduction in the level of anxiety eli- A third group of three articles20,21,24 analyzed the use of VR
cited by them and disruption of the reconsolidation of in pediatric psychology, with a specific focus on VR applica-
negative memories.39,40 Second, VR is used to facilitate the tions for the assessment of children suspected of having autism
update of existing body representations.41,42 According to a spectrum disorder57 or other neurodevelopmental disorders58,59
recent theory,43–47 eating and weight disorders may be the (e.g., attention-deficit hyperactivity disorder). In this field, dif-
outcome of a broader impairment in multisensory body in- ferent from the previous ones, the level of clinical evidence
tegration that locks the individuals to an old memory of the available is still low, even if the existing data suggest moderate
body.48 In this view, even if the subject is able to lose weight evidence about the effectiveness of VR-based treatments.24 In
after a diet, the multisensory impairment does not allow relation to this topic, another article specifically explored the
her/him to experience the new body and reduce the level of use of VR for the assessment of psychiatric disorders,4 finding
body dissatisfaction. VR allows a wrong representation that virtual worlds are able to induce and assess psychiatric
of the body to be updated through two different strategies. symptoms simultaneously, with significant correlations be-
In the first—‘‘reference frame shifting’’49,50—the subject re- tween VR measures and traditional diagnostic tools. Moreover,
experiences in VR a negative situation related to the body VR is also effective in assessing cue reactivity60: its use is able
(e.g., teasing) in both the first and third person (e.g., seeing and to increase subjective craving in smokers,61,62 alcohol drink-
supporting her/his avatar in the VR world). In the second— ers,63 eaters,64 and cocaine-dependent individuals.65
Table 1. Meta-Analyses and Systematic and Narrative Reviews Published in the Last 12 Months Related
to the Use of Virtual Reality in the Diagnosis and Treatment of Mental Health Disorders
Review type Article Included studies Conclusions (from the articles)
Systematic Riva G, Baños RM, Botella C, et al. 27 systematic ‘‘The available data support the use of this technology in the treatment
meta-review Transforming experience: the potential of reviews and of anxiety disorders, pain management, obesity and eating disorders,
augmented reality and virtual reality for meta-analyses and stress-related disorders. But still, there is no clear good quality
enhancing personal and clinical change. evidence for or against using VR for the treatment of depression and
Frontiers in Psychiatry 2016; 7:164.1 schizophrenia.’’
Systematic review (mental Freeman D, Reeve S, Robinson A, et al. 285 studies ‘‘VR environments can elicit psychiatric symptoms, manipulation of VR
health) Virtual reality in the assessment, can inform the understanding of disorders, and simpler psychological
understanding, and treatment of mental treatments can be successfully administered in VR.
health disorders. Psychological Medicine The most established finding is that VR exposure-based treatments can
2017; 47:2393–2400.2 reduce anxiety disorders, but there are numerous research and
treatment avenues of promise.’’
Reply to the above systematic Riva G. Letter to the editor: virtual reality in 3 studies ‘‘Three different RCTs have shown at 1-year follow-up that VR for
review (eating and weight the treatment of eating and weight eating and weight disorders has a higher efficacy than the gold
disorders) disorders. Psychological Medicine 2017; standard in the field, i.e. cognitive–behavioral therapy (CBT).’’
47:2567–2568.3
Narrative review (mental Mishkind MC, Norr AM, Katz AC, et al. Not reported ‘‘More research is needed before VRE may be considered standard of
health therapy) Review of virtual reality treatment in care in some areas; however, for patients with PTSD or anxiety, and
psychiatry: evidence versus current especially patients not responding or not willing to participate in
diffusion and use. Current Psychiatry traditional therapy, the use of VRE may be considered as an option.

3
Reports 2017; 19:80.19 The use of VR for other conditions such as chronic pain,
rehabilitation, and addictions also shows clinical promise.’’
Systematic review (mental van Bennekom MJ, de Koning PP, Denys D. 39 studies ‘‘Nearly all VR environments studied were able to simultaneously
health assessment) Virtual reality objectifies the diagnosis of provoke and measure psychiatric symptoms. Furthermore, in 14
psychiatric disorders: a literature review. studies, significant correlations were found between VR measures and
Frontiers in Psychiatry 2017; 8:163.4 traditional diagnostic measures. Relatively small clinical sample sizes
were used, impeding definite conclusions.’’
Narrative review (anxiety Lindner P, Miloff A, Hamilton W, et al. Not reported ‘‘While having been researched for decades and proven efficacious for
disorders) Creating state of the art, next-generation the treatment of anxiety disorders, the pending and ongoing release of
virtual reality exposure therapies for consumer-targeted VR hardware platforms signals an opportune time
anxiety disorders using consumer to develop the next generation of VR exposure therapies for
hardware platforms: design considerations widespread dissemination as self-help applications and integration
and future directions. Cognitive Behaviour into regular health care settings.’’
Therapy 2017; 46:404–420.5
Systematic review (mental Massetti T, Crocetta TB, Silva TDD, et al. 11 studies ‘‘The use of tDCS combined with VR showed positive results in both
health) Application and outcomes of therapy healthy and impaired patients including pain management. Future
combining transcranial direct current studies with larger sample sizes and homogeneous participants are
stimulation and virtual reality: a required to confirm the benefits of tDCS and VR.’’
systematic review. Disability &
Rehabilitation: Assistive Technology
2017; 12:551–559.6

(continued)
Table 1. (Continued)
Review type Article Included studies Conclusions (from the articles)
Systematic review (mental Jerdan SW, Grindle M, van Woerden HC, 82 studies ‘‘Our review demonstrated that VR is effective in provoking realistic
health) Kamel Boulos MN. Head-Mounted Virtual reactions to feared stimuli, particularly for anxiety; moreover, it
Reality and Mental Health: Critical proved that the immersive nature of VR is an ideal fit for the
Review of Current Research. JMIR management of pain. However, the lack of studies surrounding
Serious Games 2018; 6:e14. depression and stress highlight the literature gaps that still exist.’’
Systematic review and meta- Arroll B, Wallace HB, Mount V, et al. 16 studies ‘‘A range of therapies are effective for acrophobia in the short term but
analysis (acrophobia) A systematic review and meta-analysis not in the long term. Many of the comparative studies showed
of treatments for acrophobia. Med J Aust equivalence between therapies, but this finding may be due to a type II
2017; 206:263–267. statistical error. The quality of reporting was poor in most studies.’’
Narrative review (psychosis) Rus-Calafell M, Garety P, Sason E, et al. 50 studies ‘‘Virtual reality is a promising method to be used in the assessment of
Virtual reality in the assessment and neurocognitive deficits and the study of relevant clinical symptoms.
treatment of psychosis: a systematic Furthermore, preliminary findings suggest that it can be applied to the
review of its utility, acceptability and delivery of cognitive rehabilitation, social skills training interventions
effectiveness. Psychological Medicine and virtual reality-assisted therapies for psychosis.’’
2017 Jul 24 [Epub ahead of print].7
Systematic reviews (phobias) Botella C, Fernández-Álvarez J, Guillén V, et al. 11 studies ‘‘VRET applications have become an effective alternative that can equal
Recent progress in virtual reality exposure the results of traditional treatments for phobias from an efficacy point

4
therapy for phobias: a systematic review. of view. However, they are also tools capable of enhancing the
Current Psychiatry Reports 2017; 19:42.8 psychological treatment field.’’
Narrative review (anxiety Maples-Keller JL, Yasinski C, Manjin N, Not reported ‘‘VRE is consistent with models of extinction learning and provides
disorders) et al. Virtual reality-enhanced extinction several advantages for use within exposure-based interventions.
of phobias and post-traumatic stress. Broadly, extant research provides support for the effectiveness of
Neurotherapeutics 2017; 14:554–563.10 VRE in reducing symptoms of specific phobias and PTSD, with
outcomes generally superior to waitlist controls and comparable with
traditional exposure therapy.’’
Meta-analysis (flight anxiety) Cardosx RAI, David OA, David, DO. Virtual 11 studies ‘‘Results pointed out significant overall efficiency of VRET in flight
reality exposure therapy in flight anxiety: a anxiety at post-test and follow-up. Analysis highlighted the
quantitative meta-analysis. Computers in superiority of VRET vs. control conditions at post-test and follow-up
Human Behavior 2017; 72:371–380.11 and the superiority of VRET vs. classical evidence-based
interventions at post-test and follow-up.’’
Narrative review (weight Castelnuovo G, Pietrabissa G, Manzoni GM, Not reported ‘‘Another current and future scenario where CBT could be improved in
disorders) et al. Cognitive behavioral therapy to aid the management of obesity is represented by virtual reality (VR)
weight loss in obese patients: current applications, such as the VR-enhanced CBT that is a sort of enhanced
perspectives. Psychology Research & CBT of obesity with a VR module focused on unlocking the negative
Behavior Management 2017; 10:165– memory of the body, changing its dysfunctional behavioral correlates,
173.12 and managing negative emotional states.’’

(continued)
Table 1. (Continued)
Review type Article Included studies Conclusions (from the articles)
Narrative review (weight Paul L, Van Der Heiden C, Hoek HW. Not reported ‘‘Although empirical evidence is still scare, results show that CBT is
disorders) Cognitive behavioral therapy and effective in reducing disordered eating disorders and depression in
predictors of weight loss in bariatric bariatric patients. New techniques for applying CBR by virtual reality
surgery patients. Current Opinion in potentially make CBT more accessible and less costly’’
Psychiatry 2017; 30:474–479.13
Systematic review (clinical Dascal J, Reid M, Ishak WW, et al. Virtual 11 studies ‘‘Data from 11 eligible studies provide insight into three current medical
medicine) reality and medical inpatients: a applications of VR technology: pain distraction, eating disorders, and
systematic review of randomized, cognitive/motor rehabilitation. Overall, a majority of studies from the
controlled trials. Innovations in Clinical past decade found VR to be efficacious, easy to use, safe, and
Neuroscience 2017; 14:14–21.14 contributing to high patient satisfaction.’’
Systematic review and meta- Chan E, Foster S, Sambell R, Leong P. 20 studies ‘‘VR may have a role in acutely painful procedures, however included
analysis (procedural pain) Clinical efficacy of virtual reality for acute studies were clinically and statistically heterogenous. Further research
procedural pain management: A is required to validate findings, establish cost efficacy and optimal
systematic review and meta-analysis. clinical settings for usage. Future trials should report in accordance
PLoS ONE 2018; 13:e0200987. with established guidelines.’’
Narrative review (clinical Li L, Yu F, Shi D, et al. Application of virtual Not reported ‘‘VR has shown to be effective in reduction of burn-induced pain and
medicine) reality technology in clinical medicine. management of pain in other situations . Virtual reality exposure therapy
American Journal of Translational and virtual reality cognitive behavior therapy have become effective

5
Research 2017; 9:3867–3880.15 choices for patients with anxiety disorders and other phobias like fear of
flying, claustrophobia, acrophobia or generalized social phobia’’
Narrative review (mental Maples-Keller JL, Bunnell BE, Kim SJ, et al. Not reported ‘‘VR has emerged as a viable tool to help in a number of different
health) The use of virtual reality technology in the disorders, with the most strength of evidence for use in exposure
treatment of anxiety and other psychiatric therapy for patients with anxiety disorders, cue exposure therapy for
disorders. Harvard Review of Psychiatry patients with substance use disorders, and distraction for patients with
2017; 25:103–113.9 acute pain requiring painful procedures.’’
Systematic review (eating de Carvalho M, Dias T, Duchesne M, et al. 19 studies ‘‘Two different randomized, controlled trials have shown at one-year
disorders) Virtual reality as a promising strategy in follow-up that VR had a higher efficacy than the gold standard in the
the assessment and treatment of bulimia field, i.e., cognitive behavioral therapy (CBT). In conclusion, based
nervosa and binge eating disorder: a on the current available data VR-based environments may be
systematic review. Behavioral Sciences considered a promising strategy for the assessment and treatment of
2017; 7:43.17 BN and BED.’’
Systematic review (clinical Pourmand A, Davis S, Lee D, et al. 45 studies ‘‘These articles provide data, which strongly support the hypothesis that
medicine) Emerging utility of virtual reality as a VR simulations can enhance pain management (by reducing patient
multidisciplinary tool in clinical medicine. perception of pain and anxiety), can augment clinical training
Games for Health Journal 2017; 6:263– curricula and physical rehabilitation protocols (through immersive
270.18 audiovisual environments), and can improve clinical assessment of
cognitive function (through improved ecological validity).’’

(continued)
Table 1. (Continued)
Review type Article Included studies Conclusions (from the articles)
Systematic review (autism) Duffield TC, Parsons TD, Landry A, et al. 5 studies ‘‘Psychometric comparisons of these tools for the neuropsychological
Virtual environments as an assessment assessment of pediatric individuals with ASD are lacking as the
modality with pediatric ASD populations: current review demonstrated, although the use of VEs. This is a
a brief report. Child Neuropsychology particularly important area of future research considering most
2017 Sep 13 [Epub ahead of print].20 identification, and thus testing, treatment, and training occur in
childhood for ASD.’’
Narrative review (pediatrics) Parsons TD, Riva G, Parsons S, et al. Virtual Not reported ‘‘VR can offer safe, repeatable, and diversifiable interventions that can
reality in pediatric psychology. Pediatrics benefit assessments and learning in both typically developing children
2017; 140:S86–S91.21 and children with disabilities. Research has also pointed to VR’s
capacity to reduce children’s experience of aversive stimuli and
reduce anxiety levels.’’
Systematic review (autism) Mesa-Gresa P, Gil-Gomez H, Lozano-Quilis 31 studies There is moderate evidence that VR-based treatments can help children

6
JA, Gil-Gomez JA. Effectiveness of with ASD. The lack of definitive findings does not allow us to state
virtual reality for children and adolescents that VR-based treatments can improve the results of traditional
with autism spectrum disorder: an treatments. Nevertheless, the promising results and the advantages of
evidence-based systematic review. Sensors VR (especially considering ASD symptomatology) should encourage
(Basel) 2018; 18:pii:E2486. the scientific community to develop new VR-based treatments.
Systematic review (eating Clus D, Larsen ME, Lemey C, Berrouiguet 26 studies Overall, VR techniques enable the evaluation of pathological eating
disorders) S. The use of virtual reality in patients behaviors and body image distortions. In addition to CBT, use of VR
with eating disorders: systematic review. J techniques by patients with eating disorders decreased their negative
Med Internet Res 2018; 20:e157. emotional responses to virtual food stimuli or exposure to their body
shape.
NEUROSCIENCE OF VIRTUAL REALITY 7

Three final articles explored the use of VR in the assess- achieve benefit from VR therapy.92 As noted by Price and
ment and treatment of psychosis7 and in pain manage- Anderson, ‘‘The results support presence as a conduit that
ment.6,25 For psychosis, the available studies confirm the enabled phobic anxiety to be expressed during exposure to a
efficacy of VR for the multimodal assessment of cognitive virtual environment. However, presence was not supported
functioning,7 including social cognition/competence66 and as contributing to treatment outcome. This suggests feeling
hallucinations/paranoid ideations.67 For treatment, even if present during exposure may be necessary but not sufficient
the available studies are very promising,68–70 there is a lack to achieve benefit from VR exposure.’’92(p750)
of randomized controlled trials demonstrating whether VR is A new argument that is introduced and discussed in this
more efficacious or efficient than other interventions.7 article is that VR shares with the brain the same basic
In relation to the use of VR for pain management, older mechanism: embodied simulations.43,93
systematic reviews71,72 demonstrated the efficacy of VR
distraction73–75 for reducing experimental pain,76 as well as
VR as Simulative Technology
the one generated by burn injury care,77–79 chronic pain,80–82
and procedural pain.83–85 Hence, the first new one6 focused An increasingly popular hypothesis—predictive coding94–96—
its analysis on the integrated use of VR with brain stimula- suggests that the brain actively maintains an internal model
tion (transcranial direct-current stimulation) in pain man- (simulation) of the body and the space around it, which pro-
agement. Again, even if the level of clinical evidence is still vides predictions about the expected sensory input and tries to
low, a study86 demonstrated the efficacy of this approach in minimize the amount of prediction errors (or ‘‘surprise’’). An
reducing the severity of neuropathic pain and various neu- in-depth discussion of these concepts is not offered here be-
ropathic pain subtypes. Finally, the second new one,25 sug- cause authoritative and thorough accounts have been provided
gests that VR may have a role in acutely painful procedures, elsewhere.94–99 However, herein, the focus is on the concept
even if further research is required. of simulation introduced by this paradigm to understand better
Overall, this meta-review indicated that VR is a powerful the links between the brain and VR.
clinical tool for behavioral health, able to provide effective One of the main tenets of predictive coding is that to
assessment and treatment options for a variety of mental regulate and control the body in the world effectively, the
health disorders. Specifically, the 25 meta-analyses and brain creates an embodied simulation of the body in the
systematic and narrative reviews indicated that VR compares world. There are two main characteristics of this simulation.
favorably to existing treatments in anxiety disorders, eating First, different from other internal models used in cognitive
and weight disorders, and pain management, with long-term science—such as Tolman’s cognitive maps or Johhson–
effects that generalize to the real world. Moreover, they show Laird’s internal models—they are simulations of sensory
the potential of VR as assessment tool with practical appli- motor experiences. In this view, they include visceral/auto-
cations that range from social and cognitive deficits to ad- nomic (interoceptive), motor (proprioceptive), and sensory
diction. Finally, they suggest a clinical potential in the (e.g., visual, auditory) information. Second, embodied sim-
treatment of psychosis and in the pediatric field, even if there ulations reactivate multimodal neural networks, which have
is no definitive evidence for or against the use of VR. produced the simulated/expected effect before.
This approach is used not only for actions, but also for
concepts and emotions. Specifically, a concept is a group of
The Effectiveness of VR as a Clinical Tool
distributed multimodal ‘‘patterns’’ of activity across differ-
An open issue not directly addressed by most of these ent populations of neurons (motor, somatosensory, limbic,
articles is why VR is an effective clinical tool. In many and frontal areas) that support a goal achievement.100,101 So,
articles, attention is focused on the high level of control and the simulation of a concept involves its reenactment in
customization allowed by this technology.1,2,9,10,87 VR al- modality-specific brain areas. Moreover, the brain uses
lows the level of fit between the content of the exposure and emotion concepts to categorize sensations. As underlined by
the feared stimuli to be optimized. Moreover, using it, the Barrett, ‘‘That is, the brain constructs meaning by correctly
therapist has a total control—limited only by the specific anticipating (predicting and adjusting to) incoming sensa-
features of the used software—on the contents of the expe- tions. Sensations are categorized so that they are (a) ac-
rience. Finally, it offers a safer and more private context for tionable in a situated way and therefore (b) meaningful,
the patient that facilitates his/her engagement. based on past experience. When past experiences of emotion
Another important point suggested by different articles is (e.g., happiness) are used to categorize the predicted sensory
the level of ‘‘presence’’ provided by the virtual experience. array and guide action, then one experiences or perceives
In fact, VR provides a digital place to the individual where that emotion (happiness).’’100(p9) In this view, the feeling of
he/she can be placed and live a synthetic but realistic expe- presence in a space can be considered as an evolutive tool
rience.88 As noted by some colleagues, VR can be considered used to track the difference between the predicted sensations
an advanced imaginal system89,90: an advanced form of and those that are incoming from the sensory world, both
imagery that is as effective as reality in inducing experiences externally and internally.93,102,103
and emotions. For example, as demonstrated by a recent VR works in a similar way: it uses computer technology to
meta-analysis, presence and anxiety are associated with each create a simulated world that individuals can manipulate and
other during VRE therapy for the treatment of anxiety.91 This explore as if they were in it. In other words, the VR expe-
allows a level of self-reflectiveness that is both more pre- rience tries to predict the sensory consequences of your
dictable and controllable than the one offered by reality, but movements, showing to you the same scene you will see in
higher than the one provided by memory and imagination.1 the real world. Specifically, VR hardware tracks the motion
However, presence alone is necessary but not sufficient to of the user, while VR software adjusts the images on the
8 RIVA ET AL.

user’s display to reflect the changes produced by the motion of the brain117,118 by directly targeting the processes behind
in the virtual world. To achieve it, like the brain, the VR system real-world behaviors.119–121
maintains a model (simulation) of the body and the space But what is the real clinical potential of VR as an em-
around it. This prediction is then used to provide the expected bodied technology? According to neuroscience, the body
sensory input using the VR hardware. Obviously, to be realistic, matrix105,106,122,123 serves to maintain the integrity of the
the VR model tries to mimic the brain model as much as body at both the homeostatic and psychological levels by
possible: the more the VR model is similar to the brain model, supervising the cognitive and physiological resources nec-
the more the individual feels present in the VR world.93,104 essary to protect the body and the space around it. Specifically,
the body matrix plays a critical role in high-end cognitive
processes such as motivation, emotion, social cognition, and
VR as Embodied Technology
self-awareness,124–126 while exerting a top-down modulation
As has just been seen, the brain creates multiple multi- over basic physiological mechanisms such as thermoregula-
sensory simulations to predict100: (a) upcoming sensory tory control127,128 and the immune system.123
events both inside and outside the body, and (b) the best In this view, different authors114,116,129,130 have recently
action to deal with the impending sensory events. Moseley suggested that an altered functioning of the body matrix and/
et al. suggested that these simulations are integrated with or its related processes might be the cause of different neu-
sensory data in the ‘‘body matrix,’’ a coarse supramodal rological and psychiatric conditions. If this is true, VR can
multisensory representation of the body and the space around be the core of a new trans-disciplinary research field—
it.105–107 Specifically, the contents of the body matrix are embodied medicine115,116—the main goal of which is the use
defined by top-down predictive signals, integrating the of advanced technology for altering the body matrix, with the
multisensory (motor and visceromotor) simulations of the goal of improving people’s health and well-being.
causes of perceived sensory events.108 The different simu- As has been seen in the first section of this article, two
lations are then ranked and included in the body matrix ac- different VR embodiment techniques—body swapping51,52
cording to their relevance for the intentions of the self and reference frame shifting49,50—are currently used in the
(selective attention). At the same time, the content and the treatment of eating and weight disorders. The first one,
priority of the different simulations are corrected by bottom- body swapping, replaces the contents of the bodily self-
up prediction errors that signal mismatches between pre- consciousness with synthetic ones (synthetic embodiment).
dicted and actual contents of sensory events.109 This has been used in eating and weight disorders to im-
At the end of this process, the body matrix defines where prove the experience of the body in both clinical (anorexia
the self is present, that is, in the body that our brain considers and morbid obesity)131,132 and non-clinical subjects.133–135
as the most likely to be its one.110–112 As underlined by Apps Nevertheless, the potential of this approach is wider.136 For
and Tsakiris, ‘‘The mental representation of the physical example, it may offer a non-pharmacological way to reduce
properties of one’s self are, therefore, also probabilistic. That chronic pain. As has been seen in the first section of this
is, one’s own body is the one that has the highest probability article, VR distraction is effectively used to reduce acute pain.
of being ‘me,’ since other objects are probabilistically less Nevertheless, according to Tsay et al., ‘‘available findings
likely to evoke the same sensory inputs. In short, the notion present compelling evidence for a novel multisensory and
that there is a ‘self’ is the most parsimonious and accurate multimodal approach to therapies for chronic pain disor-
explanation for sensory inputs.’’110(p88) ders’’137(p249) In this view, the use of VR embodiment may
If presence in the body is the outcome of different em- offer new treatment options for pain management.138–140
bodied simulations, and VR is a simulation technology, this Some studies have suggested the possibility of using VR body
suggests the possibility of altering the experience of the body swapping to improve body perception disturbance in patients
by designing targeted virtual environments.113 In this view, with complex regional pain syndrome.141,142
VR can be defined as an ‘‘embodied technology’’ for its The second technique, reference frame shifting, structures
possibility of modifying the embodiment experience of its the individual’s bodily self-consciousness through the focus
users.114–116 As noted by Riva et al., ‘‘using VR, subjects can and reorganization of its contents (mindful embodiment).50,143
experience the synthetic environment as if it was ‘their sur- It has been successfully used in different randomized trials in
rounding world’ (incarnation: the physical body is within a patients with eating and weight disorders54,55 to update the
virtual environment) or can experience their synthetic ava- contents of their body memory. But again, its applications are
tars as if they were ‘their own body’ (embodiment: the probably wider. For example, Osimo et al. integrated body
physical body is replaced by the virtual one).’’1(p9) In other swapping (in the avatar of Sigmund Freud) and reference
words, VR is able to fool the predictive coding mechanisms frame shifting to improve mood and happiness in a non-clinical
used by the brain generating the feeling of presence in a sample.143
virtual body and in the digital space around it. A final emerging approach is the use of VR to augment the
Up to now, VR has been used to simulate external reality, bodily experience through the awareness of internal (and
that is, to make people feel ‘‘real’’ what is actually not really difficult to sense) bodily information, or the mapping of a
there (i.e., the environment). However, the ability of VR to sensory channel to a different one—for example vision to
fool the predictive coding mechanisms that regulate the ex- touch or to hearing (augmented embodiment).144,145 For ex-
perience of the body also allows it to make people feel ample, Suzuki et al.146 implemented an innovative ‘‘cardiac
‘‘real’’ what they are not. In other words, VR can offer new rubber hand illusion’’ that combined computer-generated
ways for structuring, augmenting, and/or replacing the ex- augmented reality with feedback of interoceptive informa-
perience of the body for clinical goals.114–116 Moreover, it tion. Their results showed that the virtual-hand ownership is
may offer new embodied ways for assessing the functioning enhanced by cardio-visual feedback in time with the actual
NEUROSCIENCE OF VIRTUAL REALITY 9

heartbeat, supporting the use of this technique to improve The first outcome of an integrated VR platform able to
emotion regulation. simulate both the external and the inner world is the possi-
bility of structuring, augmenting, and/or replacing all the
different experiential aspects of bodily self-consciousness,
VR as Cognitive Technology with clinical applications in the treatment of psychiatric
VR is an embodied technology for its ability to modify the disorders, such as depression151,152 or schizophrenia,153–155
experience of the body. However, the body is not simply an and neurological disorders, such as chronic pain137,156 and
object like any other; it has a special status.93,147,148 It is neglect.157,158
perceived in a multisensory way, from the outside (ex- The final long-term outcome of this possibility may be the
teroception, the body perceived through the senses) as well embodied virtual training machine described by the science-
as from within (inner body, including interoception, the fiction thriller The Matrix. In this movie, the heroes, Trinity
sense of the physiological condition of the body; proprio- and Neo, learned how to fight martial-arts battles and drive
ception, the sense of the position of the body/body segments; motorcycles and helicopters by experiencing the bodily pro-
and vestibular input, the sense of motion of the body) and cesses and concepts related to the skill through an embodied
from memory. This is true also for the simulative code used simulation.
by the brain for creating concepts. As has been seen before,
it integrates visceral/autonomic (interoceptive), motor (pro-
Conclusions
prioceptive), and sensory information. If concepts are em-
bodied simulations, and VR is an embodied technology, it The first article discussing a VR application in the field of
should be possible to facilitate cognitive modeling and behavioral health was published in 1995.159 Now, more than
change by designing targeted virtual environments able to 20 years later, VR is a reality in this field. This is the result of
modify concepts both from outside and from inside.114 a meta-review presented in this article assessing the meta-
Nevertheless, there is a critical shortcoming that at the analyses and systematic and narrative reviews published in
moment is limiting this possibility: VR simulates the exter- this field in the last 22 months. Twenty-five different articles
nal world/body but not the internal one. In fact, actual VR have demonstrated the clinical potential of this technology in
technology is very effective in reproducing the exteroceptive both the diagnosis and the treatment of mental health dis-
(external) features of the body using vision and hearing, but orders. Specifically, they indicate that VR compares favor-
less effective in reproducing the other senses (i.e., touch and ably to existing treatments in anxiety disorders, eating and
smell149). It is partially effective in reproducing the propri- weight disorders, and pain management, with long-term ef-
oceptive (motor) features of the body using haptic technol- fects that generalize to the real world.
ogies,150 but it is not yet able to reproduce the interoceptive/ But why is VR so effective? Here, the following an-
vestibular (internal) features of the body. swer is suggested: VR shares with the brain the same basic
Recently, Riva et al.116 introduced the concept of ‘‘sono- mechanism—embodied simulations.
ception,’’ a novel noninvasive technological paradigm based According to neuroscience, to regulate and control the
on wearable acoustic and vibrotactile transducers, as a pos- body in the world effectively, the brain creates an embodied
sible approach to structure, augment, and/or replace the simulation of the body in the world used to represent and
contents of the inner body. This approach should be able to predict actions, concepts, and emotions. Specifically, it is
modulate the inner body (interoception, proprioception, and used to predict: (a) upcoming sensory events both inside and
vestibular input) through the stimulation of both mechano- outside the body, and (b) the best action to deal with the
receptors in different parts of the body—the stomach, the impending sensory events.100 There are two main charac-
heart, the muscles—and the otolith organs of the vestibular teristics of this simulation. First, it simulates sensory motor
system (see Fig. 2). experiences, including visceral/autonomic (interoceptive),

FIG. 2. The technology of


‘‘sonoception.’’
10 RIVA ET AL.

motor (proprioceptive), and sensory (e.g., visual, auditory) Acknowledgments


information. Second, embodied simulations reactivate mul- This article was supported by the Italian MIUR research
timodal neural networks which have produced the simulated/ project ‘‘Unlocking the memory of the body: Virtual Reality
expected effect before. in Anorexia Nervosa’’ (201597WTTM) and by the Italian
VR works in a similar way: the VR experience tries to Ministry of Health research project ‘‘High-end and low-end
predict the sensory consequences of the individual’s move- virtual reality systems for the rehabilitation of frailty in the
ments, providing to him/her the same scene he/she will see in elderly’’ (PE-2013-0235594).
the real world. To achieve this, the VR system, like the brain,
maintains a model (simulation) of the body and the space
around it. Author Disclosure Statement
If presence in the body is the outcome of different em- No competing financial interests exist.
bodied simulations, and VR is a simulation technology, this
suggests the possibility of altering the experience of the
body by designing targeted virtual environments.113 In this References
view, VR can be defined as an ‘‘embodied technology’’ for 1. Riva G, Baños RM, Botella C, et al. Transforming expe-
its possibility of modifying the embodiment experience of rience: the potential of augmented reality and virtual re-
its users.114–116 In other words, VR is able to fool the pre- ality for enhancing personal and clinical change. Frontiers
dictive coding mechanisms used by the brain, generating the in Psychiatry 2016; 7:164.
feeling of presence in a virtual body and in the digital space 2. Freeman D, Reeve S, Robinson A, et al. Virtual reality in
around it. the assessment, understanding, and treatment of mental
Moreover, if concepts are embodied simulations, and VR health disorders. Psychological Medicine 2017; 47:2393–
is an embodied technology, it should be possible to facilitate 2400.
cognitive modeling and change by designing targeted virtual 3. Riva G. Letter to the editor: virtual reality in the treatment
environments able to modify concepts from both outside and of eating and weight disorders. Psychological Medicine
inside.114 2017; 47:2567–2568.
Nevertheless, at the moment, there is a critical shortcoming 4. van Bennekom MJ, de Koning PP, Denys D. Virtual re-
that is limiting this possibility: VR simulates the external ality objectifies the diagnosis of psychiatric disorders: a
world/body but not the internal one. Recently, Riva et al.116 literature review. Frontiers in Psychiatry 2017; 8:163.
introduced the concept of ‘‘sonoception’’ (www.sonoception. 5. Lindner P, Miloff A, Hamilton W, et al. Creating state of
the art, next-generation virtual reality exposure therapies
com), a novel noninvasive technological paradigm based on
for anxiety disorders using consumer hardware platforms:
wearable acoustic and vibrotactile transducers able to stim-
design considerations and future directions. Cognitive
ulate both mechanoreceptors in different parts of the body— Behaviour Therapy 2017; 46:404–420.
the stomach, the heart, the muscles—and the otolith organs of 6. Massetti T, Crocetta TB, Silva TDD, et al. Application
the vestibular system (see Fig. 2). The first outcome of this and outcomes of therapy combining transcranial direct
approach is the development of an interoceptive stimulator current stimulation and virtual reality: a systematic re-
that is both able to assess interoceptive time perception in view. Disability & Rehabilitation: Assistive Technology
clinical patients160 and to enhance heart rate variability (the 2017; 12:551–559.
short-term vagally mediated component—rMSSD) through 7. Rus-Calafell M, Garety P, Sason E, et al. Virtual reality in
the modulation of the subjects’ parasympathetic system.161 the assessment and treatment of psychosis: a systematic
The integration of these technologies with VR in a multi- review of its utility, acceptability and effectiveness. Psy-
sensory simulative platform will allow the modulation of both chological Medicine 2017; 48:362–391.
the external and internal bodily information, to structure, 8. Botella C, Fernández-Álvarez J, Guillén V, et al. Recent
augment and/or replace the contents of our bodily self- progress in virtual reality exposure therapy for phobias:
consciousness. a systematic review. Current Psychiatry Reports 2017; 19:42.
In conclusion, even if VR is already a reality in behavioral 9. Maples-Keller JL, Bunnell BE, Kim SJ, et al. The use of
health, the possibility of using it to simulate both the external virtual reality technology in the treatment of anxiety and
and internal world may open new clinical options in the near other psychiatric disorders. Harvard Review of Psychiatry
future able to target the experience of the body and its related 2017; 25:103–113.
processes directly. Psychosomatics is an interdisciplinary field 10. Maples-Keller JL, Yasinski C, Manjin N, et al. Virtual
that explores the relationships between psychosocial, behavioral reality-enhanced extinction of phobias and post-traumatic
stress. Neurotherapeutics 2017; 14:554–563.
factors, and bodily processes. The long-term goal of the vision
11. Cardosx RAI, David OA, David DO. Virtual reality expo-
presented in this article is the use of simulative technologies—
sure therapy in flight anxiety: a quantitative meta-analysis.
both simulating the external world and the internal one—to Computers in Human Behavior 2017; 72:371–380.
reverse engineer the psychosomatic processes that connect 12. Castelnuovo G, Pietrabissa G, Manzoni GM, et al. Cog-
mind and body. If achieved, this perspective will provide a nitive behavioral therapy to aid weight loss in obese pa-
radically new meaning to the classical Juvenal’s Latin dictum tients: current perspectives. Psychology Research &
‘‘Mens sana in corpore sano’’ (a healthy mind in a healthy Behavior Management 2017; 10:165–173.
body) by allowing a new trans-disciplinary research field— 13. Paul L, Van Der Heiden C, Hoek HW. Cognitive behav-
‘‘Embodied Medicine’’115,116—that will use advanced multi- ioral therapy and predictors of weight loss in bariatric
sensory technologies to alter bodily processes for enhancing surgery patients. Current Opinion in Psychiatry 2017; 30:
homeostasis and well-being. 474–479.
NEUROSCIENCE OF VIRTUAL REALITY 11

14. Dascal J, Reid M, Ishak WW, et al. Virtual reality and flying. Journal of Consulting & Clinical Psychology 2000;
medical inpatients: a systematic review of randomized, 68:1020–1026.
controlled trials. Innovations in Clinical Neuroscience 2017; 32. Parsons TD, Rizzo AA. Affective outcomes of virtual
14:14–21. reality exposure therapy for anxiety and specific phobias:
15. Li L, Yu F, Shi D, et al. Application of virtual reality a meta-analysis. Journal of Behavior Therapy & Experi-
technology in clinical medicine. American Journal of mental Psychiatry 2008; 39:250–261.
Translational Research 2017; 9:3867–3880. 33. Goncalves R, Pedrozo AL, Coutinho ES, et al. Efficacy of
16. Arroll B, Wallace HB, Mount V, et al. A systematic re- virtual reality exposure therapy in the treatment of PTSD:
view and meta-analysis of treatments for acrophobia. The a systematic review. PLoS One 2012; 7:e48469.
Medical Journal of Australia 2017; 206:263–267. 34. Botella C, Garcı̀a-Palacios A, Villa H, et al. Virtual reality
17. de Carvalho M, Dias T, Duchesne M, et al. Virtual reality exposure in the treatment of panic disorder and agora-
as a promising strategy in the assessment and treatment of phobia: a controlled study. Clinical Psychology & Psy-
bulimia nervosa and binge eating disorder: a systematic chotherapy 2007; 14:164–175.
review. Behavioral Sciences 2017; 7:43. 35. Anderson PL, Price M, Edwards SM, et al. Virtual reality
18. Pourmand A, Davis S, Lee D, et al. Emerging utility of exposure therapy for social anxiety disorder: a random-
virtual reality as a multidisciplinary tool in clinical med- ized controlled trial. Journal of Consulting & Clinical
icine. Games for Health Journal 2017; 6:263–270. Psychology 2013; 81:751–760.
19. Mishkind MC, Norr AM, Katz AC, et al. Review of virtual 36. Gaggioli A, Pallavicini F, Morganti L, et al. Experiential
reality treatment in psychiatry: evidence versus current virtual scenarios with real-time monitoring (interreality)
diffusion and use. Current Psychiatry Reports 2017; 19:80. for the management of psychological stress: a block ran-
20. Duffield TC, Parsons TD, Landry A, et al. Virtual envi- domized controlled trial. Journal of Medical Internet Re-
ronments as an assessment modality with pediatric ASD search 2014; 16:e167.
populations: a brief report. Child Neuropsychology 2017 37. Repetto C, Gaggioli A, Pallavicini F, et al. Virtual reality
Sep 13 [Epub ahead of print]; DOI: 10.1080/09297049 and mobile phones in the treatment of generalized anxiety
.2017.1375473. disorders: a Phase-2 clinical trial. Personal & Ubiquitous
21. Parsons TD, Riva G, Parsons S, et al. Virtual reality in Computing 2013; 17:253–260.
pediatric psychology. Pediatrics 2017; 140:S86–S91. 38. Wiederhold BK, Riva G, Gutierrez-Maldonado J. Virtual
22. Jerdan SW, Grindle M, van Woerden HC, Kamel Boulos reality in the assessment and treatment of weight-related
MN. Head-mounted virtual reality and mental health: disorders. Cyberpsychology, Behavior, & Social Net-
critical review of current research. JMIR Serious Games working 2016; 19:67–73.
2018; 6:e14. 39. Pla-Sanjuanelo J, Ferrer-Garcı́a M, Vilalta-Abella F, et al.
23. Clus D, Larsen ME, Lemey C, Berrouiguet S. The use of Testing virtual reality-based cue-exposure software: which
virtual reality in patients with eating disorders: systematic cue-elicited responses best discriminate between patients
review. Journal of Medical Internet Research 2018; 20:e157. with eating disorders and healthy controls? Eating and
24. Mesa-Gresa P, Gil-Gomez H, Lozano-Quilis JA, Gil- Weight Disorders 2017 Jul 27 [Epub ahead of print]; DOI:
Gomez JA. Effectiveness of virtual reality for children and 10.1007/s40519-017-0419-4.
adolescents with autism spectrum disorder: an evidence- 40. Ferrer-Garcia M, Gutierrez-Maldonado J, Pla-Sanjuanelo
based systematic review. Sensors 2018; 18:pii:E2486. J, et al. A randomised controlled comparison of second-
25. Chan E, Foster S, Sambell R, Leong P. Clinical efficacy of level treatment approaches for treatment-resistant adults
virtual reality for acute procedural pain management: a with bulimia nervosa and binge eating disorder: assessing
systematic review and meta-analysis. PLoS One 2018; 13: the benefits of virtual reality cue exposure therapy. Eu-
e0200987. ropean Eating Disorders Review 2017; 25:479–490.
26. Rothbaum BO, Rizzo AS, Difede J. Virtual reality expo- 41. Riva G. Modifications of body image induced by virtual
sure therapy for combat-related posttraumatic stress dis- reality. Perceptual & Motor Skills 1998; 86:163–170.
order. Annals of the New York Academy of Sciences 2010; 42. Riva G, Bacchetta M, Baruffi M, et al. Virtual reality-based
1208:126–132. experiential cognitive treatment of obesity and binge-eating
27. Wiederhold BK, Wiederhold MD. Three-year follow-up disorders. Clinical Psychology & Psychotherapy 2000; 7:
for virtual reality exposure for fear of flying. CyberPsy- 209–219.
chology & Behavior 2003; 6:441–445. 43. Riva G, Gaudio S. Locked to a wrong body: eating dis-
28. McLay RN, Wood DP, Webb-Murphy JA, et al. A ran- orders as the outcome of a primary disturbance in multi-
domized, controlled trial of virtual reality-graded expo- sensory body integration. Consciousness & Cognition
sure therapy for post-traumatic stress disorder in active 2018; 59:57–59.
duty service members with combat-related post-traumatic 44. Riva G, Gaudio S, Dakanalis A. The neuropsychology of
stress disorder. Cyberpsychology, Behavior, & Social self objectification. European Psychologist 2015; 20:34–43.
Networking 2011; 14:223–239. 45. Riva G. Out of my real body: cognitive neuroscience
29. Repetto C, Gorini A, Vigna C, et al. The use of biofeed- meets eating disorders. Frontiers in Human Neuroscience
back in clinical virtual reality: the INTREPID project. 2014; 8:236.
Journal of Visualized Experiments 2009 Nov 12 [Epub 46. Riva G. Neuroscience and eating disorders: the allocentric
ahead of print]; DOI: 10.3791/1554. lock hypothesis. Medical Hypotheses 2012; 78:254–257.
30. Wiederhold BK, Wiederhold MD. Clinical observations 47. Serino S, Dakanalis A, Gaudio S, et al. Out of body, out of
during virtual reality therapy for specific phobias. Cy- space: impaired reference frame processing in eating
berPsychology & Behavior 1999; 2:161–168. disorders. Psychiatry Research 2015; 230:732–734.
31. Rothbaum BO, Hodges L, Smith S, et al. A controlled 48. Riva G, Dakanalis A. Altered processing and integration
study of virtual reality exposure therapy for the fear of of multisensory bodily representations and signals in
12 RIVA ET AL.

eating disorders: a possible path toward the understanding 65. Saladin ME, Brady KT, Graap K, et al. A preliminary
of their underlying causes. Frontiers in Human Neu- report on the use of virtual reality technology to elicit
roscience 2018; 12:49. craving and cue reactivity in cocaine dependent individ-
49. Akhtar S, Justice LV, Loveday C, et al. Switching memory uals. Addictive Behaviors 2006; 31:1881–1894.
perspective. Consciousness & Cognition 2017; 56:50–57. 66. Gutiérrez-Maldonado J, Rus-Calafell M, Marquez-Rejón
50. Riva G. The key to unlocking the virtual body: virtual re- S, et al. Associations between facial emotion recognition,
ality in the treatment of obesity and eating disorders. Journal cognition and alexithymia in patients with schizophrenia:
of Diabetes Science & Technology 2011; 5:283–292. comparison of photographic and virtual reality presenta-
51. Normand JM, Giannopoulos E, Spanlang B, et al. Multi- tions. Studies in Health Technology & Informatics 2012;
sensory stimulation can induce an illusion of larger belly 181:88–92.
size in immersive virtual reality. Plos One 2011; 6:e16128. 67. Stinson K, Valmaggia LR, Antley A, et al. Cognitive
52. Gutiérrez-Maldonado J, Wiederhold BK, Riva G. Future triggers of auditory hallucinations: an experimental in-
directions: how virtual reality can further improve the vestigation. Journal of Behavioral Therapy & Experi-
assessment and treatment of eating disorders and obesity. mental Psychiatry 2010; 41:179–184.
Cyberpsychology, Behavior, & Social Networking 2016; 68. Freeman D, Bradley J, Antley A, et al. Virtual reality in the
19:148–153. treatment of persecutory delusions: randomised controlled
53. Marco JH, Perpina C, Botella C. Effectiveness of cogni- experimental study testing how to reduce delusional con-
tive behavioral therapy supported by virtual reality in the viction. British Journal of Psychiatry 2016; 209:62–67.
treatment of body image in eating disorders: one year 69. Gega L, White R, Clarke T, et al. Virtual environments
follow-up. Psychiatry Research 2013; 209:619–625. using video capture for social phobia with psychosis.
54. Manzoni GM, Cesa GL, Bacchetta M, et al. Virtual Cyberpsychogy, Behavior, & Social Networking 2013; 16:
reality-enhanced cognitive–behavioral therapy for morbid 473–479.
obesity: a randomized controlled study with 1 year follow- 70. Leff J, Williams G, Huckvale MA, et al. Computer-
up. Cyberpsychology, Behavior, & Social Networking 2016; assisted therapy for medication-resistant auditory hallu-
19:134–140. cinations: proof-of-concept study. British Journal of Psy-
55. Cesa GL, Manzoni GM, Bacchetta M, et al. Virtual reality chiatry 2013; 202:428–433.
for enhancing the cognitive behavioral treatment of obe- 71. Malloy KM, Milling LS. The effectiveness of virtual re-
sity with binge eating disorder: randomized controlled ality distraction for pain reduction: a systematic review.
study with one-year follow-up. Journal of Medical Inter- Clinical Psychology Review 2010; 30:1011–1018.
net Research 2013; 15:e113. 72. Morris LD, Louw QA, Grimmer-Somers K. The effec-
56. Marta F-G, Joana P-S, Antonios D, et al. A randomized tiveness of virtual reality on reducing pain and anxiety in
trial of virtual reality-based cue exposure second-level burn injury patients: a systematic review. The Clinical
therapy and cognitive behavior second-level therapy for Journal of Pain 2009; 25:815–826.
bulimia nervosa and binge-eating disorder: outcome at 73. Wiederhold BK, Soomro A, Riva G, et al. Future direc-
six-month followup. Cyberpsychology, Behavior, & Social tions: advances and implications of virtual environments
Networking 2018 July 30 [Epub ahead of print]; DOI: designed for pain management. Cyberpsychology, Beha-
10.1089/cyber.2017.0675. vior, & Social Networking 2014; 17:414–422.
57. Parsons S. Authenticity in virtual reality for assessment 74. Sulea C, Soomro A, Boyd C, et al. Pain management in
and intervention in autism: a conceptual review. Educa- virtual reality: a comprehensive research chart. Cyberpsy-
tional Research Review 2016; 19:138–157. chology, Behavior, & Social Networking 2014; 17:402–413.
58. Negut A, Jurma AM, David D. Virtual-reality-based at- 75. Li A, Montano Z, Chen VJ, et al. Virtual reality and pain
tention assessment of ADHD: ClinicaVR: classroom-CPT management: current trends and future directions. Pain
versus a traditional continuous performance test. Child Management 2011; 1:147–157.
Neuropsychology 2017; 23:692–712. 76. Keefe FJ, Huling DA, Coggins MJ, et al. Virtual reality
59. Pollak Y, Weiss PL, Rizzo AA, et al. The utility of a for persistent pain: a new direction for behavioral pain
continuous performance test embedded in virtual reality in management. Pain 2012; 153:2163–2166.
measuring ADHD-related deficits. Journal of Develop- 77. Schmitt YS, Hoffman HG, Blough DK, et al. A random-
mental & Behavioral Pediatrics 2009; 30:2–6. ized, controlled trial of immersive virtual reality analgesia,
60. Hone-Blanchet A, Wensing T, Fecteau S. The use of during physical therapy for pediatric burns. Burns 2011;
virtual reality in craving assessment and cue-exposure 37:61–68.
therapy in substance use disorders. Frontiers in Human 78. Hoffman HG, Richards TL, Coda B, et al. Modulation of
Neuroscience 2014; 8:844. thermal pain-related brain activity with virtual reality:
61. Bordnick PS, Graap KM, Copp HL, et al. Virtual reality evidence from fMRI. Neuroreport 2004; 15:1245–1248.
cue reactivity assessment in cigarette smokers. CyberP- 79. Hoffman HG, Richards TL, Van Oostrom T, et al. The
sychology & Behavior 2005; 8:487–492. analgesic effects of opioids and immersive virtual reality
62. Lee J, Lim Y, Graham SJ, et al. Nicotine craving and cue distraction: evidence from subjective and functional brain
exposure therapy by using virtual environments. CyberP- imaging assessments. Anesthesia & Analgesia 2007; 105:
sychology & Behavior 2004; 7:705–713. 1776–1783, table of contents.
63. Bordnick PS, Traylor A, Copp HL, et al. Assessing re- 80. Wiederhold BK, Gao K, Sulea C, et al. Virtual reality as a
activity to virtual reality alcohol based cues. Addictive distraction technique in chronic pain patients. Cyberpsy-
Behaviors 2008; 33:743–756. chology, Behavior, & Social Networking 2014; 17:346–
64. Ledoux T, Nguyen AS, Bakos-Block C, et al. Using vir- 352.
tual reality to study food cravings. Appetite 2013; 71:396– 81. Parsons TD, Trost Z. (2014) Virtual reality graded expo-
402. sure therapy as treatment for pain-related fear and
NEUROSCIENCE OF VIRTUAL REALITY 13

disability in chronic pain. In Ma M, Jain L, Anderson P, 99. Clark A. (2016) Surfing uncertainty: prediction, ac-
eds. Virtual, augmented reality and serious games for tion, and the embodied mind. Oxford: Oxford University
healthcare 1. Intelligent Systems Reference Library, vol. Press.
68. Berlin: Springer, pp. 523–546. 100. Barrett LF. The theory of constructed emotion: an active
82. Jin W, Choo A, Gromala D, et al. A virtual reality game inference account of interoception and categorization.
for chronic pain management: a randomized, controlled Social Cognitive & Affective Neuroscience 2017; 12:1–
clinical study. Studies in Health Technology & Infor- 23.
matics 2016; 220:154–160. 101. Barsalou LW. Situated simulation in the human concep-
83. Hua Y, Qiu R, Yao WY, et al. The effect of virtual reality tual system. Language & Cognitive Processes 2003; 18:
distraction on pain relief during dressing changes in 513–562.
children with chronic wounds on lower limbs. Pain 102. Riva G, Waterworth JA, Waterworth EL, et al. From in-
Management Nursing 2015; 16:685–691. tention to action: the role of presence. New Ideas in
84. Wiederhold MD, Gao K, Wiederhold BK. Clinical use of Psychology 2011; 29:24–37.
virtual reality distraction system to reduce anxiety and 103. Riva G, Mantovani F. From the body to the tools and
pain in dental procedures. Cyberpsychology, Behavior, & back: a general framework for presence in mediated in-
Social Networking 2014; 17:359–365. teractions. Interacting with Computers 2012; 24:203–210.
85. Mosso-Vazquez JL, Gao K, Wiederhold BK, et al. Virtual 104. Sanchez-Vives MV, Slater M. From presence to con-
reality for pain management in cardiac surgery. Cyberp- sciousness through virtual reality. Nature Reviews Neuro-
sychology, Behavior, & Social Networking 2014; 17:371– science 2005; 6:332–339.
378. 105. Moseley GL, Gallace A, Spence C. Bodily illusions in
86. Soler MD, Kumru H, Pelayo R, et al. Effectiveness of health and disease: physiological and clinical perspectives
transcranial direct current stimulation and visual illusion and the concept of a cortical ‘‘body matrix.’’ Neuro-
on neuropathic pain in spinal cord injury. Brain 2010; 133: science & Biobehavioral Reviews 2012; 36:34–46.
2565–2577. 106. Gallace A, Spence C. (2014) In touch with the future: the
87. Pallavicini F, Ferrari A, Zini A, et al. (2017) What dis- sense of touch from cognitive neuroscience to virtual re-
tinguishes a traditional gaming experience from one in ality. Oxford: Oxford University Press.
virtual reality? An exploratory study. In Ahram T, Falcão 107. Sedda A, Tonin D, Salvato G, et al. Left caloric vestibular
C, eds. Advances in human factors in wearable technol- stimulation as a tool to reveal implicit and explicit pa-
ogies and game design. Cham, Switzerland: Springer, rameters of body representation. Consciousness & Cog-
pp. 225–231. nition 2016; 41:1–9.
88. Riva G, Botella C, Baños R, et al. (2015) Presence- 108. Friston K, Daunizeau J, Kilner J, et al. Action and be-
inducing media for mental health applications. In Lombard havior: a free-energy formulation. Biological Cybernetics
M, Biocca F, Freeman J, et al., eds. Immersed in media. 2010; 102:227–260.
New York: Springer, pp. 283–332. 109. Friston K. The free-energy principle: a rough guide to the
89. Vincelli F, Riva G. Virtual reality as a new imaginative brain? Trends in Cognitive Sciences 2009; 13:293–301.
tool in psychotherapy. Studies in Health Technology & 110. Apps MA, Tsakiris M. The free-energy self: a predictive
Informatics 2000; 70:356–358. coding account of self-recognition. Neuroscience & Bio-
90. Riva G, Molinari E, Vincelli F. Interaction and presence in behavioral Reviews 2014; 41:85–97.
the clinical relationship: virtual reality (VR) as commu- 111. Holmes NP, Spence C. The body schema and the multi-
nicative medium between patient and therapist. IEEE sensory representation(s) of peripersonal space. Cognitive
Transactions on Information Technology in Biomedicine Processing 2004; 5:94–105.
2002; 6:198–205. 112. Serino S, Scarpina F, Dakanalis A, et al. The role of age
91. Ling Y, Nefs HT, Morina N, et al. A meta-analysis on the on multisensory bodily experience: an experimental study
relationship between self-reported presence and anxiety in with a virtual reality full-body illusion. Cyberpsychology,
virtual reality exposure therapy for anxiety disorders. Behavior, & Social Networking 2018; 21:304–310.
PLoS One 2014; 9:e96144. 113. Oliveira ECD, Bertrand P, Lesur MER, et al. Virtual body
92. Price M, Anderson P. The role of presence in virtual re- swap: a new feasible tool to be explored in health and
ality exposure therapy. Journal of Anxiety Disorders 2007; education. In 2016 XVIII Symposium on Virtual and
21:742–751. Augmented Reality (SVR 2016). New York: Institute of
93. Riva G. The neuroscience of body memory: from the self Electrical and Electronics Engineers, pp. 81–89.
through the space to the others. Cortex 2017 Jul 25 [Epub 114. Riva G. From virtual to real body: virtual reality as em-
ahead of print]; DOI: 10.1016/j.cortex.2017.07.013. bodied technology. Journal of Cybertherapy & Re-
94. Friston K. The free-energy principle: a unified brain the- habiliation 2008; 1:7–22.
ory? Nature Reviews Neuroscience 2010; 11:127–138. 115. Riva G. (2016) Embodied medicine: what human com-
95. Friston K. Embodied inference and spatial cognition. puter confluence can offer to health care. In Gaggioli A,
Cognitive Processing 2012; 13:S171–177. Ferscha A, Riva G, et al., eds. Human computer conflu-
96. Clark A. Whatever next? Predictive brains, situated ence: transforming human experience through symbi-
agents, and the future of cognitive science. Behavioral & otic technologies. Warsaw, Poland: De Gruyter Open,
Brain Sciences 2013; 36:181–204. pp. 55–79.
97. Talsma D. Predictive coding and multisensory integration: 116. Riva G, Serino S, Di Lernia D, et al. Embodied medicine:
an attentional account of the multisensory mind. Frontiers mens sana in corpore virtuale sano. Frontiers in Human
in Integrative Neuroscience 2015; 9:19. Neuroscience 2017; 11:120.
98. Hohwy J. (2013) The predictive mind. Oxford: Oxford 117. Parsons TD. Virtual reality for enhanced ecological validity
University Press. and experimental control in the clinical, affective and social
14 RIVA ET AL.

neurosciences. Frontiers in Human Neuroscience 2015; 9: cating altered body representation. Neuroscience & Bio-
660. behavioral Reviews 2015; 52:221–232.
118. Parsons T, Gaggioli A, Riva G. Virtual reality for research 138. Romano D, Llobera J, Blanke O. Size and viewpoint of an
in social neuroscience. Brain Sciences 2017; 7:42. embodied virtual body impact the processing of painful
119. Serino S, Baglio F, Rossetto F, et al. Picture Interpretation stimuli. Journal of Pain 2016; 17:350–358.
Test (PIT) 360: an innovative measure of executive 139. Pazzaglia M, Haggard P, Scivoletto G, et al. Pain and
functions. Scientific Reports 2017; 7:16000. somatic sensation are transiently normalized by illusory
120. Cipresso P. Modeling behavior dynamics using compu- body ownership in a patient with spinal cord injury. Re-
tational psychometrics within virtual worlds. Frontiers in storative Neurology & Neuroscience 2016; 34:603–613.
Psychology 2015; 6:1725. 140. Sarig Bahat H, Takasaki H, Chen XQ, et al. Cervical ki-
121. Cipresso P, Serino S, Riva G. Psychometric assessment nematic training with and without interactive VR training
and behavioral experiments using a free virtual reality for chronic neck pain—a randomized clinical trial. Man-
platform and computational science. BMC Medical In- ual Therapy 2015; 20:68–78.
formatics & Decision Making 2016; 16:37. 141. Hwang H, Cho S, Lee JH. The effect of virtual body
122. Finotti G, Migliorati D, Costantini M. Multisensory inte- swapping with mental rehearsal on pain intensity and body
gration, bodily self-consciousness and disorders of the im- perception disturbance in complex regional pain syndrome.
mune system. Brain, Behavior, & Immunity 2015; 49:e31. International Journal of Rehabilitation Research 2014; 37:
123. Finotti G, Costantini M. Multisensory body representation 167–172.
in autoimmune diseases. Scientific Reports 2016; 6:21074. 142. Jeon B, Cho S, Lee JH. Application of virtual body
124. Tsakiris M. The multisensory basis of the self: from body swapping to patients with complex regional pain syn-
to identity to others. Quarterly Journal of Experimental drome: a pilot study. Cyberpsychology, Behavior, & So-
Psychology 2017; 70:597–609. cial Networking 2014; 17:366–370.
125. Maister L, Slater M, Sanchez-Vives MV, et al. Changing 143. Osimo SA, Pizarro R, Spanlang B, et al. Conversations
bodies changes minds: owning another body affects social between self and self as Sigmund Freud—a virtual body
cognition. Trends in Cognitive Sciences 2015; 19:6–12. ownership paradigm for self counselling. Scientific Re-
126. Maister L, Sebanz N, Knoblich G, et al. Experiencing ports 2015; 5.
ownership over a dark-skinned body reduces implicit ra- 144. Waterworth JA, Waterworth EL. (2014) Altered, ex-
cial bias. Cognition 2013; 128:170–178. panded and distributed embodiment: the three stages of
127. Macauda G, Bertolini G, Palla A, et al. Binding body and interactive presence. In Riva G, Waterworth JA, Murray
self in visuo-vestibular conflicts. European Journal of D, eds. Interacting with presence: HCI and the sense of
Neuroscience 2015; 41:810–817. presence in computer-mediated environments. Berlin: De
128. Gallace A, Soravia G, Cattaneo Z, et al. Temporary inter- Gruyter Open, pp. 36–50.
ference over the posterior parietal cortices disrupts ther- 145. Duquette P. Increasing our insular world view: interocep-
moregulatory control in humans. PLoS One 2014; 9:e88209. tion and psychopathology for psychotherapists. Frontiers
129. Brugger P, Lenggenhager B. The bodily self and its dis- in Neuroscience 2017; 11:135.
orders: neurological, psychological and social aspects. 146. Suzuki K, Garfinkel SN, Critchley HD, et al. Multisensory
Current Opinion in Neurology 2014; 27:644–652. integration across exteroceptive and interoceptive do-
130. Tsakiris M, Critchley H. Interoception beyond homeo- mains modulates self-experience in the rubber-hand illu-
stasis: affect, cognition and mental health. Philosophical sion. Neuropsychologia 2013; 51:2909–2917.
Transactions of the Royal Society B 2016; 371. 147. Aspell JE, Lenggenhager B, Blanke O. (2012) Multi-
131. Keizer A, van Elburg A, Helms R, et al. A virtual reality sensory perception and bodily self-consciousness. From
full body illusion improves body image disturbance in out-of-body to inside-body experience. In Murray MM,
anorexia nervosa. PLoS One 2016; 11:e0163921. Wallace MT, eds. The neural bases of multisensory pro-
132. Serino S, Scarpina F, Keizer A, et al. A novel technique cesses. Boca Raton, FL: CRC Press, ch. 24.
for improving bodily experience in a non-operable 148. Blanke O. Multisensory brain mechanisms of bodily self-
super-super obesity case. Frontiers in Psychology 2016; consciousness. Nature Reviews Neuroscience 2012; 13:
7:837. 556–571.
133. Serino S, Pedroli E, Keizer A, et al. Virtual reality body 149. Serrano B, Baños RM, Botella C. Virtual reality and
swapping: a tool for modifying the allocentric memory of stimulation of touch and smell for inducing relaxation: a
the body. Cyberpsychology, Behavior, & Social Net- randomized controlled trial. Computers in Human Beha-
working 2016; 19:127–133. vior 2016; 55:1–8.
134. Preston C, Ehrsson HH. Illusory changes in body size 150. Adams RJ, Hannaford B. Control law design for haptic
modulate body satisfaction in a way that is related to non- interfaces to virtual reality. IEEE Transactions on Control
clinical eating disorder psychopathology. Plos One 2014; Systems Technology 2002; 10:3–13.
9:e85773. 151. Barrett LF, Quigley KS, Hamilton P. An active inference
135. Preston C, Ehrsson HH. Illusory obesity triggers body theory of allostasis and interoception in depression. Phi-
dissatisfaction responses in the insula and anterior cin- losophical Transactions of the Royal Society B 2016; 371.
gulate cortex. Cerebral Cortex 2016; 26:4450–4460. 152. Wheatley J, Brewin CR, Patel T, et al. I’ll believe it when
136. Serino S, Dakanalis A. Bodily illusions and weight-related I can see it: imagery rescripting of intrusive sensory
disorders: clinical insights from experimental research. memories in depression. Journal of Behavior Therapy &
Annals of Physical & Rehabilitation Medicine 2017; 60: Experimental Psychiatry 2007; 38:371–385.
217–219. 153. Postmes L, Sno HN, Goedhart S, et al. Schizophrenia as a
137. Tsay A, Allen TJ, Proske U, et al. Sensing the body in self-disorder due to perceptual incoherence. Schizophrenia
chronic pain: a review of psychophysical studies impli- Research 2014; 152:41–50.
NEUROSCIENCE OF VIRTUAL REALITY 15

154. Ferri F, Costantini M, Salone A, et al. Upcoming tactile 160. Di Lernia D, Serino S, Pezzulo G, et al. Feel the time.
events and body ownership in schizophrenia. Schizo- Time perception as a function of interoceptive processing.
phrenia Research 2014; 152:51–57. Frontiers in Human Neuroscience 2018; 12:74.
155. Klaver M, Dijkerman HC. Bodily experience in schizo- 161. Di Lernia D, Cipresso P, Pedroli E, Riva G. Toward an
phrenia: factors underlying a disturbed sense of body own- embodied medicine: a portable device with programmable
ership. Frontiers in Human Neuroscience 2016; 10:305. interoceptive stimulation for heart rate variability en-
156. Di Lernia D, Serino S, Riva G. Pain in the body. Altered hancement. Sensors 2018; 18:pii:E2469.
interoception in chronic pain conditions: A systematic 162. Uman LS. Systematic reviews and meta-analyses. Journal
review. Neuroscience & Biobehavioral Reviews 2016; 71: of the Canadian Academy of Child & Adolescent Psy-
328–341. chiatry 2011; 20:57–59.
157. Bolognini N, Convento S, Casati C, et al. Multisensory
integration in hemianopia and unilateral spatial neglect:
evidence from the sound induced flash illusion. Neu- Address correspondence to:
ropsychologia 2016; 87:134–143. Prof. Giuseppe Riva
158. Lenggenhager B, Loetscher T, Kavan N, et al. Paradoxical Department of Psychology
extension into the contralesional hemispace in spatial Università Cattolica del Sacro Cuore
neglect. Cortex 2012; 48:1320–1328. Largo Gemelli 1
159. Rothbaum BO, Hodges LF, Kooper R, et al. Effectiveness 20123, Milan
of computer-generated (virtual reality) graded exposure in Italy
the treatment of acrophobia. American Journal of Psy-
chiatry 1995; 152:626–628. E-mail: giuseppe.riva@unicatt.it

You might also like